Protein disulfide isomerase: The multifunctional redox chaperone of the endoplasmic reticulum

Seminars in Cell and Developmental Biology

Volumn 10, Issue 5, 1999, Pages 481-493

  Noiva, Robert ^a  

^a UNIVERSITY OF SOUTH DAKOTA   (United States)

Author keywords

Endoplasmic reticulum; Microsomal triglyceride transfer protein; Prolyl 4 hydroxylase; Protein disulfide isomerase; Protein thiol oxidoreductase

Indexed keywords

CHAPERONE; OXIDOREDUCTASE; PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE; PROTEIN DISULFIDE ISOMERASE;

ABETALIPOPROTEINEMIA; CHEMICAL MODEL; CHEMISTRY; ENDOPLASMIC RETICULUM; ENZYMOLOGY; GENE EXPRESSION REGULATION; METABOLISM; PROTEIN BINDING; PROTEIN TERTIARY STRUCTURE; REVIEW;

ABETALIPOPROTEINEMIA; ENDOPLASMIC RETICULUM; GENE EXPRESSION REGULATION, ENZYMOLOGIC; MODELS, CHEMICAL; MOLECULAR CHAPERONES; OXIDOREDUCTASES; PROCOLLAGEN-PROLINE DIOXYGENASE; PROTEIN BINDING; PROTEIN DISULFIDE-ISOMERASE; PROTEIN STRUCTURE, TERTIARY;

EID: 0033210414     PISSN: 10849521     EISSN: None     Source Type: Journal    
DOI: 10.1006/scdb.1999.0319     Document Type: Article

References (111)

1. Goldberger RF, Epstein CJ, Anfinsen CB. Acceleration of the reactivation of reduced bovine pancreatic ribonuclease by a microsomal system from rat liver. J Biol Chem. 238:1963;628-635.
2. Edman JC, Ellis L, Blacher RW, Roth RA, Rutter WJ. Sequence of protein disulphide isomerase and implications of its relationship to thioredoxin. Nature. 317:1985;267-270.
3. Kemmink J, Darby NJ, Dijkstra K, Nilges M, Creighton TE. The folding catalyst protein disulfide isomerase is constructed of active and inactive thioredoxin modules. Current Biology. 7:1997;239-245.
4. Ren B, Tibbelin G, dePascale D, Rossi M, Bartolucci S, Ladenstein R. A protein disulfide isomerase from the archaeon Pyrococcus furiosus contains two thioredoxin fold units. Nature Struct Biol. 5:1998;602-611.
5. 15N NMR spectroscopy. Biochemistry. 35:1996;7684-7691.
6. Darby NJ, Kemmink J, Creighton TE. Identifying and characterizing a structural domain of protein disulfide isomerase. Biochemistry. 35:1996;10517-10528.
7. Thompson J, Sack J, Jamil, H, Wetterau, J, Einspahr H, Banaszak L. Structure of the microsomal triglyceride transfer protein in complex with protein disulfide isomerase. FASEB J. 12:1998.
8. Gilbert HF. Molecular and cellular aspects of thiol-disulfide exchange. Adv Enzymol. 63:1990;69-172.
9. Hawkins HC, Freedman RB. The reactivities and ionization properties of the active site dithiol groups of mammalian protein disulphide isomerase. Biochem J. 275:1991;335-339.
10. Lundstrom J, Holmgren A. Determination of the reduction-oxidation potential of the thioredoxin-like domains of protein disulfide-isomerase fr om the equilibrium with glutathione and thioredoxin. Biochemistry. 32:1993;6649-6655.
11. Vouri K, Myllylä R, Pihlajaniemi T, Kivirikko K. Expression and site-directed mutagenesis of human protein disulfide isomerase in Escherichia coli. J Biol Chem. 267:1992;7211-7214.
12. LaMantia M, Lennarz WJ. The essential function of yeast protein disulfide isomerase does not reside in its isomerase activity. Cell. 74:1993;899-908.
13. Laboissière MCA, Sturley SL, Raines RT. The essential function of protein disulfide isomerase is to unscramble non-native disulfide bonds. J Biol Chem. 270:1995;28006-28009.
14. Hawkins HC, Blackburn EC, Freedman RB. Comparison of the activities of protein disuphide-isomerase and thioredoxin in catalyzing disulphide isomerization in a protein substrate. Biochem J. 275:1991;349-353.
15. Lu X, Gilbert HF, Harper JW. Conserved residues flanking the thiol/disulfide centers of protein disulfide isomerase are not essential for catalysis of thiol/disulfide exchange. Biochemistry. 30:1992;4205-4210.
16. Krause G, Lundström J, Barea JL, de la Cuesta CP, Holmgren A. Mimicking the active site of protein disulfide-isomerase by substitution of proline 34 in Escherichia coli thioredoxin. J Biol Chem. 266:1991;9494-9500.
17. Creighton TE, Zapun A, Darby NJ. Mechanisms and catalysts of disulfide bond formation in proteins. Trends Biotechnol. 13:1995;18-23.
18. Lundström J, Holmgren A. Protein disulfide-isomerase is a substrate for thioredoxin reductase and has thioredoxin-like activity. J Biol Chem. 265:1990;9114-9120.
19. Darby NJ, Freedman RB, Creighton TE. Dissecting the mechanism of protein disulfide isomerase: Catalysis of disulfide bond formation in a model peptide. Biochemistry. 33:1994;7937-7947.
20. Hwang C, Sinskey AJ, Lodish HF. Oxidized redox state of glutathi one in the endoplasmic reticulum. Science. 257:1992;1496-1501.
21. Pollard MG, Travers KJ, Weissman JS. Ero1p: a novel and ubiquitous protein with an essential role in oxidative protein folding in the endoplasmic reticulum. Mol Cell. 1:1998;171-182.
22. Frand AR, Kaiser CA. The ERO1 gene of yeast is required for oxidation of protein dithiols in the endoplasmic reticulum. Mol Cell. 1:1998;161-170.
23. Lyles MM, Gilbert HF. Mutations in the thioredoxin sites of protein disulfide isomerase reveal functional non-equivalence of the N- and C-terminal domains. J Biol Chem. 269:1994;30946-30952.
24. Darby NJ, Creighton TE. Functional properties of the individual thioredoxin-like domains of protein disulfide isomerase. Biochemistry. 34:1995;11725-11735.
25. Koivunen P, Pirneskoski A, Karvonen P, Ljung J, Helaakoski T, Notbohm H, Kivirikko KI. The acidic C-terminal domain of protein disulfide isomerase is not critical for the enzyme subunit function or for the chaperone or disulfide isomerase activities of the polypeptide. EMBO J. 18:1999;65-74.
26. Puig A, Primm TP, Surendran R, Lee JC, Ballard KD, Orkiszewski RS, Makarov V, Gilbert HF. A 21-kDa C-terminal fragment of protein-disulfide isomerase has isomerase, chaperone, and anti-chaperone activities. J Biol Chem. 272:1997;32988-32994.
27. Darby NJ, Penka E, Vincentelli R. The multi-domain structure of protein disulfide isomerase is essential for high catalytic activity. J Mol Biol. 276:1998;239-247.
28. Cai H, Wang CC, Tsou CL. Chaperone-like activity of protein disulfide isomerase in the refolding of a protein with no disulfide bonds. J Biol Chem. 269:1994;24550-24552.
29. Song JL, Wang CC. Chaperone-like activity of protein disulfide-isomerase in the refolding of rhodanese. Eur J Biochem. 231:1995;312-316.
30. Quan H, Fan GB, Wang CC. Indepedence of the chaperone activity of protein disulfide isomerase from its thioredoxin-like active site. J Biol Chem. 270:1995;17078-17080.
31. Dai Y, Wang CC. A mutant truncated protein disulfide isomerase with no chaperone activity. J Biol Chem. 272:1997;27572-27576.
32. Puig A, Gilbert HF. Protein disulfide isomerase exhibits chapero ne and anti-chaperone activity in the oxidative refolding of lysozyme. J Biol Chem. 269:1994;7764-7771.
33. Primm TP, Walker KW, Gilbert HF. Facilitated protein aggregation. Effects of calcium on the chaperone and anti-chaperone activity of protein disulfide-isomerase. J Biol Chem. 271:1996;33664-33669.
34. Braakman I, Helenius J, Helenius A. Role of ATP and disulphide bonds during protein folding in the endoplasmic reticulum. Nature. 356:1992;260-262.
35. Braakman I, Helenius J, Helenius A. Manipulating disulfide bond formation and protein folding in the endoplasmic reticulum. EMBO J. 11:1992;1717-1722.
36. Tatu U, Braakman I, Helenius A. Membrane glycoprotein folding, oligomerization and intracellular transport: effects of dithiothreitol in living cells. EMBO J. 12:1993;2151-2157.
37. Koivu J, Myllylä R, Helaakoski T, Pihlajaniemi T, Tasanen K, Kivirikko KI. A single polypeptide acts both as the β subunit of prolyl 4-hydroxylase and as a protein disulfide-isomerase. J Biol Chem. 262:1987;6447-6449.
38. John DCA, Grant ME, Bulleid NJ. Cell-free synthesis and assembly of prolyl 4-hydroxylase: the role of the β-subunit (PDI) in preventing misfolding and aggregation of the α-subunit. EMBO J. 12:1993;1587-1592.
39. Myllyharju J, Kivirikko KI. Identification of a novel proline-rich peptide-binding domain in prolyl 4-hydroxylase. EMBO J. 18:1999;306-312.
40. Myllyharju J, Kivirikko KI. Characterization of the iron- and 2-oxoglutarate-binding sites of human prolyl 4-hydroxylase. EMBO J. 16:1997;1173-1180.
41. Kivirikko KI, Pihlajaniemi T. Collagen hydroxylases and the protein disulfide isomerase subunit of prolyl 4-hydroxylases. Adv Enzymol Rel Areas Mol Biol. 72:1998;325-398.
42. Helaakoski T, Annunen P, Vouri K, MacNeil IA, Pihlajaniemi T, Kivirikko KI. Cloning, baculovirus expression, and characterization of a second mouse prolyl 4-hydroxylase alpha-subunit isoform: formation of an α-2 β-2 tetramer with the protein disulfide-isomerase/ β subunit. Proc Natl Acad Sci USA. 92:1995;4427-4431.
43. Veijola J, Pihlajaniemi T, Kivirikko KI. Co-expression of the -subunit of human prolyl 4-hydroxylase with BiP polypeptide in insect cells leads to the formation of soluble and insoluble complexes. Soluble -subunit-BiP complexes have no prolyl 4-hydroxylase activity. Biochem J. 315:1996;613-618.
44. Noiva R, Onodera S, Schwaller M, Irwin W. The peptide binding site of protein disulfide isomerase, Guzman N A,. Prolyl-4-Hydroxylase, Protein Disulfide Isomerase, and Other Structurally-Related Proteins. 1998;369-397 Marcel Dekker, New York.
45. Vourela A, Myllyharju J, Nissi R, Pihlajaniemi T, Kivirikko KI. Assembly of human prolyl 4-hydroxylase and type III collagen in the yeast Pichis pastoris: formation of a stable enzyme tetramer requires coexpression with collagen and assembly of a stable collagen requires coexpression with prolyl 4-hydroxylase. EMBO J. 16:1997;6702-6712.
46. Wilson R, Lees JF, Bulleid NJ. Protein disulfide isomerase acts as a molecular chaperone during the assembly of procollagen. J Biol Chem. 273:1998;9637-9643.
47. Munro S, Pelham HR. A C-terminal signal prevents secretion of luminal ER proteins. Cell. 48:1987;899-907.
48. Wetterau J, Combs KA, McLean LR, Spinner SN, Aggerbeck LP. Protein disulfide isomerase appears necessary to maintain the catalytically active structure of the microsomal triglyceride transfer protein. Biochemistry. 30:1991;9728-9735.
49. Mann CJ, Anderson TA, Read J, Chester SA, Harrison GB, Kochl S, Ritchie PJ, Bradbury P, Hussain FS, Amey J, Vanloo B, Rosseneu M, Infante R, Hancock JM, Levitt DG, Banaszak LJ, Scott J, Shoulders CC. The structure of vitellogenin provides a molecular model for the assembly and secretion of atherogenic lipoproteins. J Mol Biol. 285:1999;391-408.
50. Ricci B, Sharp D, O'Rourke E, Kienzle B, Blinderman L, Gordon D, Smith-Monroy C, Robinson G, Gregg RE, Rader DJ, Wetterau JR. A 30-amino acid truncation of the microsomal triglyceride transfer protein large subunit disrupts its interaction with protein disulfide-isomerase and causes abetalipoproteinemia. J Biol Chem. 270:1995;14281-14285.
51. Hussain MM, Bakillah A, Jamil H. Apolipoprotein B binding to microsomal triglyceride transfer protein decreases with increases in length and lipidation: implications in lipoprotein biosynthesis. Biochemistry. 36:1997;13060-13067.
52. Hussain MM, Bakillah A, Nayak N, Shelness GS. Amino acids 430-570 in apolipoprotein B are critical for its binding to microsomal triglyceride transfer protein. J Biol Chem. 273:1998;25612-25615.
53. Bradbury P, Mann CJ, Kochl S, Anderson TA, Chester SA, Hancock JM, Ritchie PJ, Amey J, Harrison GB, Levitt DG, Banaszak LJ, Scott J, Shoulders CC. A common binding site on the microsomal triglyceride transfer protein for apolipoprotein B and protein disulfide isomerase. J Biol Chem. 274:1999;3159-3164.
54. Wu X, Zhou M, Huang LS, Wetterau JR, Ginsberg HN. Demonstration of a physical interaction between microsomal triglyceride transfer protein and apolipoprotein B during the assembly of apoB-containing lipoproteins. J Biol Chem. 271:1996;10277-10281.
55. Lamberg A, Jauhiainen M, Metso J, Ehnholm C, Shoulders C, Scott J, Pihlajaniemi T, Kivirikko KI. The role of protein disulphide isomerase in the microsomal triacylglycerol transfer protein does not reside in its isomerase activity. Biochem J. 315:1996;533-536.
56. Wang L, Fast DG, Attie AD. The enzymatic and non-enzymatic roles of protein-disulfide isomerase in apoliporotein B secretion. J Biol Chem. 272:1997;27644-27651.
57. Chandrashekar R, Tsuji N, Morales T, Ozols V, Mehta K. An ERp60-like protein from the filarial parasite Dirofilaria immitis has both transglutaminase and protein disulfide isomerase activity. Proc Natl Acad Sci USA. 95:1998;531-536.
58. Macer DR, Koch GL. Identification of a set of calcium-binding proteins in the reticuloplasm, the luminal content of the endoplasmic reticulum. J Cell Sci. 91:1988;61-70.
59. Lebeche D, Lucero HA, Kaminer B. Calcium binding properties of rabbit liver protein disulfide isomerase. Biochem Biophys Res Commun. 202:1994;556-561.
60. Zapun A, Creighton TE, Rowling PJE, Freedman RB. Folding in vitro of bovine pancreatic trypsin inhibitor in the presence of proteins of the endoplasmic reticulum. Proteins. 14:1992;10-15.
61. Rupp K, Birnbach U, Lundstrom J, Van PN, Soling HD. Effects of CABP2, the rat analog of Erp72, and of CaBP1 on the refolding of denatured reduced proteins. J Biol Chem. 269:1994;2501-2507.
62. Lucero HA, Kaminer B. The role of calcium on the activity of ERcalcistorin/protein-disulfide isomerase and the significance of the C-terminal and its calcium binding. A comparison with mammalian protein-disulfide isomerase. J Biol Chem. 274:1999;3243-3251.
63. 2integrin-mediated lymphocyte adhesion by bacitracin. J Immunol. 161:1998;6323-6329.
64. Farwell AP, Lynch RM, Okulicz WC, Comi AM, Leonard JL. The actin cytoskeleton mediates the hormonally regulated translocation of type II iodothyronine 5′-deiodinase in astrocytes. J Biol Chem. 265:1991;18546-18553.
65. Safran M, Farwell A, Leonard JL. Thyroid hormone-dependent redistribution of the 55 kilodalton monomer of protein disulfide isomerase in cultured glial cells. Endocrinology. 131:1992;2413-2418.
66. Lammert E, Stevanovi S, Brunner J, Rammensee HG, Schild H. Protein disulfide isomerase is the dominant acceptor for peptides translocated into the endoplasmic reticulum. Eur J Immunol. 27:1997;1685-1690.
67. Spee P, Neefjes J. TAP-translocated peptides specifically bind proteins in the endoplasmic reticulum, including gp96, protein disulfide isomerase and calreticulin. Eur J Immunol. 27:1997;2441-2449.
68. Noiva R, Freedman RB, Lennarz WJ. Peptide binding to protein disulfide isomerase occurs at a site distinct from the active sites. J Biol Chem. 268:1993;19210-19217.
69. Puig A, Lyles MM, Noiva R, Gilbert HF. The role of the thiol/disulfide centers and peptide binding site in the chaperone and anti-chaperone activity of protein disulfide isomerase. J Biol Chem. 269:1994;19128-19135.
70. Klappa P, Ruddock LW, Darby N, Freedman RB. The b′ domain provides the principle peptide binding site of protein disulfide isomerase but all domains contribute to binding of misfolded proteins. EMBO J. 17:1998;927-935.
71. Srivastava PK, DeLeo AB, Old LJ. Tumor rejection antigens of chemically-induced sarcomas of inbred mice. Proc Natl Acad Sci USA. 83:1986;3407-3411.
72. Pelham HRB. The Florey lecture, 1992. The secretion of protein by cells. Proc Royal Soc London B. 250:1992;1-10.
73. Booth C, Koch GLE. Perturbation of cellular calcium induces secretion of luminal ER proteins. Cell. 59:1989;729-737.
74. Akagi S, Yamamoto A, Yoshimori T, Masaki R, Ogawa R, Tashiro Y. Localization of protein disulfide isomerase on plasma membranes in rat exocrine pancreatic cells. J Histochem Cytochem. 36:1988;1069-1074.
75. Essex DW, Chen K, Swiatkowska M. Localization of protein disulfide isomerase to the external surface of the platelet plasma membrane. Blood. 86:1995;2168-2173.
76. Safran M, Leonard JL. Characterization of a N -bromoacetyl- l -thyroxine affinity-labeled 55 kilodalton protein as protein disulfide isomera se in cultured glial cells. Endocrinology. 129:1991;2011-2016.
77. Bassuk JA, Capodici C, Berg RA. Protein disulfide isomerase from human periperal blood neutrophils. J Cell Physiol. 144:1990;280-286.
78. Yamauchi K, Yamamoto T, Hayashi H, Koya S, Takokawa H, Toyoshima K, Ho riuchi R. Sequence of the membrane-associated thyroid hormone binding protein from bovine liver: its identity with protein disulfide isomerase. Biochem Biophys Res Comm. 146:1987;1485-1492.
79. Terada K, Manchikalapudi P, Noiva R, Jauregui HO, Stockert RJ, Schilsky ML. Secretion, surface localization, turnover and steady state expression of protein disulfide isomerase in rat hepatocytes. J Biol Chem. 270:1995;20410-20416.
80. Yoshimori T, Semba T, Takemoto H, Akagi S, Yamamoto A, Tashiro Y. Protein disulfide-isomerase in rat exocrine pancreatic cells is exported from the endoplasmic reticulum despite possessing the retention signal. J Biol Chem. 265:1990;15984-15990.
81. Yokoi T, Nagayama S, Kajiwara R, Kawaguchi Y, Horiuchi R, Kamataki T (. dentification of protein disulfide isomerase and calreticulin as autoimmune antigens in LEC strain of rats. Biochim Biophys Acta. 1158:1993;339-344.
82. Nagayama S, Yokoi T, Kawaguchi Y, Kamataki T. Occurrence of autoantibody to protein disulfide isomerase in patients with hepatic disorder. J Toxicol Sci. 19:1994;163-169.
83. Kröning H, Kähne T, Ittensson A, Franke A, Ansorge S. Thiol-protein disulfide-oxidoreductase (protein disulfide isomerase): a new plasma membrane constituent of mature human B lymphocytes. Scan J Immunol. 39:1994;346-350.
84. Täger M, Kröning H, Thiel U, Ansorge S. Membrane-bound protein disulfide isomerase (PDI) is involved in regulation of surface expression of thiols and drug sensitivity of B-CLL. Exp Hematol. 25:1997;601-607.
85. Mandel R, Ryser HJP, Ghani F, Wu M, Peak D. Inhibition of a reductive function of the plasma membrane by bacitracin and antibodies against protein disulfide-isomerase. Proc Natl Acad Sci USA. 90:1993;4112-4116.
86. Orlandi PA. Protein-disulfide isomerase-mediated reduction of the A subunit of cholera toxin in a human intestinal cell line. J Biol Chem. 272:1997;4591-4599.
87. Majoul I, Ferrari D, Söling HD. Reduction of protein disulfide bonds in an oxidizing environment: the disulfide bridge of cholera toxin A-subunit is reduced in the endoplasmic reticulum. FEBS Lett. 401:1997;104-108.
88. Chen K, Lin Y, Detwiler TC. Protein disulfide isomerase activity is released by activated platelets. Blood. 79:1992;2226-2228.
89. Chen K, Detwiler TC, Essex DW. Characterization of protein disulphide isomerase released from activated platelets. Br J Haematol. 90:1995;425-431.
90. Hotchkiss KA, Chesterman CN, Hogg PJ. Catalysis of disulfide isomerization in thrombospondin 1 by protein disulfide isomerase. Biochemistry. 35:1996;9761-9767.
91. Huang EM, Detwiler TC, Milev Y, Essex DW. Thiol-disulfide isomerization in thrombospondin: effects of conformation and protein disulfide isomerase. Blood. 89:1997;3205-3212.
92. Tedder TF. Cell-surface receptor shedding: a means of regulating function. Am J Respir Cell Mol Biol. 5:1991;305-306.
93. Couët J, de Bernard S, Loosfelt H, Saunier B, Milgrom E, Misrahi M. Cell surface protein disulfide-isomerase is involved in the shedding of human thyrotropin receptor ectodomain. Biochemistry. 35:1996;14800-14805.
94. Clive DR, Greene JJ. Association of protein disulfide isomerase activity and the induction of contact inhibition. Exper Cell Res. 214:1994;139-144.
95. Tasanen K, Parkkonen T, Chow LT, Kivirikko KI, Pihlajaniemi T. Characterization of the human gene for a polypeptide that acts as both the β-subunit of the prolyl 4-hydroxylase and as the protein disulfide isomerase. J Biol Chem. 263:1988;16218-16224.
96. McCauliffe DP, Yang YS, Wilson J, Sontheimer RD, Capra JD. The 5′-flanking region of the human calreticulin gene shares homology with the human GRP78, GRP94, and protein disulfide isomerase promoters. J Biol Chem. 267:1992;2557-2562.
97. Marcus N, Shaffer D, Farrar P,Green M. Tissue distribution of three members of the murine protein disulfide isomerase (PDI) family. Biochim Biophys Acta. 1309:1996;253-260.
98. 2. Biochem Biophys Res Comm. 220:1996;264-268.
99. Mira E, Castaño JG. Regulation of protein disulfide isomerase gene expression in brain and liver during rat development. Biochem Biophys Res Comm. 170:1990;421-425.
100. Nieto A, Mira E, Castaño JG. Transcriptional regulation of rat liver protein disulphide-isomerase gene by insulin and in diabetes. Biochem J. 267:1990;317-323.
101. Hensel G, Abmann V, Kern HF. Hormonal regulation of protein disulfide isomerase and chaperone synthesis in the rat exocrine pancreas. Eur J Cell Biol. 63:1994;208-218.
102. Dhahbi JM, Mote PL, Tillman JB, Walford RL, Spindler SR. Dietary energy tissue specifically regulates endoplasmic reticulum chaperone gene expression in the liver of mice. J Nutrition. 127:1997;1758-1764.
103. Greene JJ, Brophy CI. Induction of protein disulfide isomerase during proliferation arrest and differentiation of SH5Y neuroblastoma cells. Cell Molec Biol. 41:1995;473-480.
104. Miyashi O, Kozaki K, Iida K, Isobe K, Hashizume Y, Saga S. Elevated expression of PDI family proteins during differentiation of mouse F9 teratocarcinoma cells. J Cellular Biochem. 68:1998;436-445.
105. Paver JL, Freedman RB, Parkhouse RME. Induction of protein disulphide-isomerase during lymphocyte activation and maturation. Biochem Soc Trans. 16:1988;56.
106. Bini L, Magi B, Marzocchi B, Arcuri F, Tripodi S, Cintorino M, Sanchez JC, Frutiger S, Hughes G, Pallini V, Hochstrasser DF, Tosi P. Protein expression profiles in human ductal carcinoma and histologically normal tissue. Electrophoresis. 18:1997;2832-2841.
107. Morrison JJ, Charnock-Jones DS, Smith SK. Messenger RNA encoding thiol protein disulphide isomerase in amnion, choion and placenta in human term and preterm labor. Br J Obstet Gynaecol. 103:1996;873-878.
108. 2+agonists on molecular chaperones in human umbilical vein endothelial cells. Electrophoresis. 16:1995;1205-1214.
109. Sun Y, Oberley LW. Redox regulation of transcriptional activators. Free Radic Biol Med. 21:1996;335-348.
110. Clive DR, Greene JJ. Cooperation of protein disulfide isomerase and redox environment in the regulation of NF-κB and AP1 binding to DNA. Cell Biochem Function. 14:1996;49-55.
111. Kim J, Mayfield SP. Protein disulfide isomerase as a regulator of chloroplast translational activation. Science. 278:1997;1954-1957.